Kumar Sampath A, Albrecht Tomáš, Kauzál Ondřej, Tomášek Oldřich
Institute of Vertebrate Biology, Czech Academy of Sciences, Brno, Czechia.
Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czechia.
Front Cell Dev Biol. 2021 Mar 29;9:638501. doi: 10.3389/fcell.2021.638501. eCollection 2021.
The fatty acid composition of biological membranes has been hypothesised to be a key molecular adaptation associated with the evolution of metabolic rates, ageing, and life span - the basis of the membrane pacemaker hypothesis (MPH). MPH proposes that highly unsaturated membranes enhance cellular metabolic processes while being more prone to oxidative damage, thereby increasing the rates of metabolism and ageing. MPH could, therefore, provide a mechanistic explanation for trade-offs between longevity, fecundity, and metabolic rates, predicting that short-lived species with fast metabolic rates and higher fecundity would have greater levels of membrane unsaturation. However, previous comparative studies testing MPH provide mixed evidence regarding the direction of covariation between fatty acid unsaturation and life span or metabolic rate. Moreover, some empirical studies suggest that an n-3/n-6 PUFA ratio or the fatty acid chain length, rather than the overall unsaturation, could be the key traits coevolving with life span. In this study, we tested the coevolution of liver fatty acid composition with maximum life span, annual fecundity, and basal metabolic rate (BMR), using a recently published data set comprising liver fatty acid composition of 106 avian species. While statistically controlling for the confounding effects of body mass and phylogeny, we found no support for long life span evolving with low fatty acid unsaturation and only very weak support for fatty acid unsaturation acting as a pacemaker of BMR. Moreover, our analysis provided no evidence for the previously reported links between life span and n-3 PUFA/total PUFA or MUFA proportion. Our results rather suggest that long life span evolves with long-chain fatty acids irrespective of their degree of unsaturation as life span was positively associated with at least one long-chain fatty acid of each type (i.e., SFA, MUFA, n-6 PUFA, and n-3 PUFA). Importantly, maximum life span, annual fecundity, and BMR were associated with different fatty acids or fatty acid indices, indicating that longevity, fecundity, and BMR coevolve with different aspects of fatty acid composition. Therefore, in addition to posing significant challenges to MPH, our results imply that fatty acid composition does not pose an evolutionary constraint underpinning life-history trade-offs at the molecular level.
生物膜的脂肪酸组成被认为是一种关键的分子适应性变化，与代谢率、衰老和寿命的进化相关——这是膜起搏器假说（MPH）的基础。MPH提出，高度不饱和的膜在促进细胞代谢过程的同时，更容易受到氧化损伤，从而加快代谢和衰老的速度。因此，MPH可以为寿命、繁殖力和代谢率之间的权衡提供一种机制性解释，预测代谢率快、繁殖力高的短命物种的膜不饱和程度会更高。然而，之前检验MPH的比较研究在脂肪酸不饱和度与寿命或代谢率之间协变方向上提供了不一致的证据。此外，一些实证研究表明，n-3/n-6多不饱和脂肪酸比例或脂肪酸链长度，而非总体不饱和度，可能是与寿命共同进化的关键特征。在本研究中，我们利用最近发表的包含106种鸟类肝脏脂肪酸组成的数据集，检验了肝脏脂肪酸组成与最大寿命、年繁殖力和基础代谢率（BMR）的共同进化关系。在对体重和系统发育的混杂效应进行统计控制后，我们发现没有证据支持低脂肪酸不饱和度与长寿共同进化，仅有非常微弱的证据支持脂肪酸不饱和度作为BMR的起搏器。此外，我们的分析没有为之前报道的寿命与n-3多不饱和脂肪酸/总多不饱和脂肪酸或单不饱和脂肪酸比例之间的联系提供证据。我们的结果反而表明，长寿与长链脂肪酸共同进化，而不论其不饱和度如何，因为寿命与每种类型（即饱和脂肪酸、单不饱和脂肪酸、n-6多不饱和脂肪酸和n-3多不饱和脂肪酸）的至少一种长链脂肪酸呈正相关。重要的是，最大寿命、年繁殖力和BMR与不同的脂肪酸或脂肪酸指数相关，表明寿命、繁殖力和BMR与脂肪酸组成的不同方面共同进化。因此，我们的结果除了给MPH带来重大挑战外，并暗示脂肪酸组成在分子水平上并非构成生命史权衡的进化限制因素。
